Skip to main content
SpringerLink
Log in

Cephalopods in the diet of nonbreeding black-browed and grey-headed albatrosses from South Georgia

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The food and feeding ecology of albatrosses during the nonbreeding season is still poorly known, particularly with regard to the cephalopod component. This was studied in black-browed Thalassarche melanophris and grey-headed T. chrysostoma albatrosses by analysing boluses collected shortly after adults returned to colonies at Bird Island, South Georgia (54°S, 38°W), in 2009. Based on stable isotopic analyses of the lower beaks, we determined the habitat and trophic level (from δ13C and δ15N, respectively) of the most important cephalopods and assessed the relative importance of scavenging in terms of the albatrosses’ feeding regimes. Based on lower rostral lengths (LRLs), the main cephalopod species in the diets of both albatrosses was Kondakovia longimana, by frequency of occurrence (F > 90 %), number (N > 40 %) and mass (M > 80 %). The large estimated mass of many squid, including K. longimana, suggests that a high proportion (>80 % by mass) was scavenged, and that scavenging is much more important during the nonbreeding season than would be expected from breeding-season diets. The diversity of cephalopods consumed by nonbreeding birds in our study was similar to that recorded during previous breeding seasons, but included two new species [Moroteuthis sp. B (Imber) and ?Mastigoteuthis A (Clarke)]. Based on similarities in LRL, δ13C and δ15N, the squid consumed may have been from the same oceanic populations or region, with the exception of Taonius sp. B (Voss) and K. longimana, which, based on significant differences in δ15N values, suggest that they may have originated from different stocks, indicating differences in the albatrosses’ feeding regimes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arata J, Xavier JC (2003) The diet of black-browed albatrosses at the Diego Ramirez Islands, Chile. Polar Biol 26:638–647. doi:10.1007/s00300-003-0530-z

    Article  Google Scholar 

  • Arata J, Robertson G, Valencia J, Xavier JC, Moreno CA (2004) Diet of grey-headed albatrosses at the Diego Ramírez Islands, Chile: ecological implications. Antarct Sci 16:263–275. doi:10.1017/S095410200400207X

    Article  Google Scholar 

  • Arkhipkin AI, Laptikhovsky VV (2008) Discovery of the fourth species of the enigmatic chiroteuthid squid Asperoteuthis (Cephalopoda: Oegopsida) and extension of the range of the genus to the South Atlantic. J Molluscan Stud 74:203–207. doi:10.1093/mollus/eyn007

    Article  Google Scholar 

  • Brown CR, Klages NT (1987) Seasonal and annual variation in diets of Macaroni (Eudyptes chrysolophus chrysolophus) and Southern rockhopper (E. chrysocome chrysocome) penguins at sub-Antarctic Marion Island. J Zool 212:7–28. doi:10.1111/j.1469-7998.1987.tb05111.x

    Article  Google Scholar 

  • Cherel Y, Hobson KA (2005) Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proc R Soc Lond B Biol Sci 272:1601–1607. doi:10.1098/rspb.2005.3115

    Article  Google Scholar 

  • Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287. doi:10.3354/meps329281

    Article  CAS  Google Scholar 

  • Cherel Y, Klages N (1998) A review of the food of albatrosses. In: Robertson G, Gales R (eds) Albatross Biology and Conservation. Surrey Beatty & Sons, Chipping Norton, pp 113–136

    Google Scholar 

  • Cherel Y, Weimerskirch H (1999) Spawning cycle of onychoteuthid squids in the southern Indian Ocean: new information from seabird predators. Mar Ecol Prog Ser 188:93–104. doi:10.3354/meps188093

    Article  Google Scholar 

  • Cherel Y, Hobson KA, Weimerskirch H (2000a) Using stable-isotope analysis of feathers to distinguish moulting and breeding origins of seabirds. Oecologia 122:155–162. doi:10.1007/pl00008843

    Article  Google Scholar 

  • Cherel Y, Weimerskirch H, Trouve C (2000b) Food and feeding ecology of the neritic-slope forager black-browed albatross and its relationships with commercial fisheries in Kerguelen waters. Mar Ecol Prog Ser 207:183–199. doi:10.3354/meps207183

    Article  Google Scholar 

  • Cherel Y, Weimerskirch H, Trouve C (2002) Dietary evidence for spatial foraging segregation in sympatric albatrosses (Diomedea spp.) rearing chicks at Iles Nuageuses, Kerguelen. Mar Biol 141:1117–1129. doi:10.1007/s00227-002-0907-5

    Article  Google Scholar 

  • Cherel Y, Duhamel G, Gasco N (2004) Cephalopod fauna of subantarctic islands: new information from predators. Mar Ecol Prog Ser 266:143–156. doi:10.3354/meps266143

    Article  Google Scholar 

  • Cherel Y, Gasco N, Duhamel G (2011) Top predators and stable isotopes document the cephalopod fauna and its trophic relationships in Kerguelen waters. In: Duhamel G, Welsford D (eds) The Kerguelen Plateau: marine ecosystem and fisheries, Proceedings of the 1st international Science Symposium on the Kerguelen Plateau. Société Française d’Ichtyologie, Abbeville, pp 99–108

    Google Scholar 

  • Cherel Y, Jaeger A, Alderman R, Jaquemet S, Richard P, Wanless RM, Phillips RA, Thompson DR (2013) A comprehensive isotopic investigation of habitat preferences in nonbreeding albatrosses from the Southern Ocean. Ecography 36:277–286. doi:10.1111/j.1600-0587.2012.07466.x

    Article  Google Scholar 

  • Cherel Y, Jaquemet S, Maglio A, Jaeger A (2014) Differences in δ13C and δ15N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations. Mar Biol 161:229–237. doi:10.1007/s00227-013-2314-5

    Article  Google Scholar 

  • Clarke MR (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, Oxford

    Google Scholar 

  • Collins MA, Rodhouse PG (2006) Southern Ocean Cephalopods. In: Alan J. Southward CMY, Lee AF (eds) Adv Mar Biol. Academic Press, pp 191–265

  • Connan M, McQuaid C, Bonnevie B, Smale M, Cherel Y, Klages N (2014) Combined stomach content, lipid and stable isotope analyses reveal spatial and trophic partitioning among three sympatric albatrosses from the Southern Ocean. Mar Ecol Prog Ser 497:259–272. doi:10.3354/meps10606

    Article  CAS  Google Scholar 

  • Croxall JP, Prince PA (1994) Dead or alive, night or day: how do albatrosses catch squid? Antarct Sci 6:155–162. doi:10.1017/S0954102094000246

    Article  Google Scholar 

  • Croxall JP, Prince PA (1996) Cephalopods as Prey. I. Seabirds. Philos Trans R Soc Lond Ser B Biol Sci 351:1023–1043. doi:10.1098/rstb.1996.0091

    Article  Google Scholar 

  • Croxall JP, Silk JR, Phillips RA, Afanasyev V, Briggs DR (2005) Global circumnavigations: tracking year-round ranges of nonbreeding albatrosses. Science 307:249–250. doi:10.1126/science.1106042

    Article  CAS  PubMed  Google Scholar 

  • Furness BL, Laugksch RC, Duffy DC (1984) Cephalopod beaks and studies of seabird diets. Auk 101:619–620

    Google Scholar 

  • González AF, Trathan PN, Yau C, Rodhouse PG (1997) Interactions between oceanography, ecology and fishery biology of the ommastrephid squid Martialia hyadesi in the South Atlantic. Mar Ecol Prog Ser 152:205–215. doi:10.3354/meps152205

    Article  Google Scholar 

  • Hobson KA, Cherel Y (2006) Isotopic reconstruction of marine food webs using cephalopod beaks: new insight from captively raised Sepia officinalis. Can J Zool 84:766–770. doi:10.1139/z06-049

    Article  Google Scholar 

  • Lu CC, Williams R (1994) Contribution to the biology of squid in the Prydz Bay region, Antarctica. Antarct Sci 6:223–229. doi:10.1017/S0954102094000349

    Google Scholar 

  • Nel DC, Lutjeharms JRE, Pakhomov EA, Ansorge IJ, Ryan PG, Klages NTW (2001) Exploitation of mesoscale oceanographic features by grey-headed albatross Thalassarche chrysostoma in the southern Indian Ocean. Mar Ecol Prog Ser 217:15–26. doi:10.3354/meps217015

    Article  Google Scholar 

  • Phillips RA, Silk JR, Phalan B, Catry P, Croxall JP (2004) Seasonal sexual segregation in two Thalassarche albatross species: competitive exclusion, reproductive role specialization or foraging niche divergence? Proc R Soc Lond B Biol Sci 271:1283–1291. doi:10.1098/rspb.2004.2718

    Article  CAS  Google Scholar 

  • Phillips RA, Silk JRD, Croxall JP, Afanasyev V, Bennett VJ (2005) Summer distribution and migration of nonbreeding albatrosses: individual consistencies and implications for conservation. Ecology 86:2386–2396. doi:10.1890/04-1885

    Article  Google Scholar 

  • Phillips R, Bearhop S, McGill RR, Dawson D (2009) Stable isotopes reveal individual variation in migration strategies and habitat preferences in a suite of seabirds during the nonbreeding period. Oecologia 160:795–806. doi:10.1007/s00442-009-1342-9

    Article  PubMed  Google Scholar 

  • Phillips R, McGill RR, Dawson D, Bearhop S (2011) Sexual segregation in distribution, diet and trophic level of seabirds: insights from stable isotope analysis. Mar Biol 158:2199–2208. doi:10.1007/s00227-011-1725-4

    Article  Google Scholar 

  • Piatkowski U, Pütz K, Heinemann H (2001) Cephalopod prey of king penguins (Aptenodytes patagonicus) breeding at Volunteer Beach, Falkland Islands, during austral winter 1996. Fish Res 52:79–90. doi:10.1016/S0165-7836(01)00232-6

    Article  Google Scholar 

  • Poncet S, Robertson G, Phillips RA, Lawton K, Phalan B, Trathan PN, Croxall JP (2006) Status and distribution of wandering, black-browed and grey-headed albatrosses breeding at South Georgia. Polar Biol 29:772–781. doi:10.1007/s00300-006-0114-9

    Article  Google Scholar 

  • Prince PA (1980) The food and feeding ecology of grey-headed albatross Diomedea chrysostoma and black-browed albatross D. melanophris. Ibis 122:476–488. doi:10.1111/j.1474-919X.1980.tb00902.x

    Article  Google Scholar 

  • Richoux N, Jaquemet S, Bonnevie B, Cherel Y, McQuaid C (2010) Trophic ecology of grey-headed albatrosses from Marion Island, Southern Ocean: insights from stomach contents and diet tracers. Mar Biol 157:1755–1766. doi:10.1007/s00227-010-1448-y

    Article  Google Scholar 

  • Rodhouse PG (1997) Precautionary measures for a new fishery on Martialia hyadesi (Cephalopoda, Ommastrephidae) in the Scotia Sea: an ecological approach. CCAMLR Sci 4:125–139

    Google Scholar 

  • Rodhouse PG, Prince PA (1993) Cephalopod prey of the black-browed albatross Diomedea melanophrys at South Georgia. Polar Biol 13:373–376. doi:10.1007/bf01681978

    Article  Google Scholar 

  • Rodhouse PG, Yeatman J (1990) Redescription of Martialia hyadesi Rochebrune and Mabille, 1889 (Mollusca: Cephalopoda) from the Southern Ocean. Bull Br Mus Nat Hist (Zool) 56:135–143

    Google Scholar 

  • Rodhouse PG, Prince PA, Clarke MR, Murray AWA (1990) Cephalopod prey of the grey-headed albatross Diomedea chrysostoma. Mar Biol 104:353–362. doi:10.1007/bf01314337

    Article  Google Scholar 

  • Schimmelmann A, DeNiro MJ (1988) Stable isotope studies on Chitin. II. The 13C/12C and 15N/14N ratios in arthropod chitin. Contrib Mar Sci 29:113–130

    Google Scholar 

  • Stowasser G, Atkinson A, McGill RAR, Phillips RA, Collins MA, Pond DW (2012) Food web dynamics in the Scotia Sea in summer: a stable isotope study. Deep Sea Res Part 2 Top Stud Oceanogr 59–60:208–221. doi:10.1016/j.dsr2.2011.08.004

    Article  Google Scholar 

  • Waugh SM, Weimerskirch H, Cherel Y, Shankar U, Prince PA, Sagar PM (1999) Exploitation of the marine environment by two sympatric albatrosses in the Pacific Southern Ocean. Mar Ecol Prog Ser 177:243–254. doi:10.3354/meps177243

    Article  Google Scholar 

  • Wolf N, Carleton SA, Martínez del Rio C (2009) Ten years of experimental animal isotopic ecology. Funct Ecol 23:17–26. doi:10.1111/j.1365-2435.2009.01529.x

    Article  Google Scholar 

  • Xavier JC, Cherel Y (2009) Cephalopod beak guide for the Southern Ocean. British Antarctic Survey, Cambridge

    Google Scholar 

  • Xavier JC, Croxall JP (2007) Predator-prey interactions: why do larger albatrosses eat bigger squid? J Zool 271:408–417. doi:10.1111/j.1469-7998.2006.00224.x

    Article  Google Scholar 

  • Xavier JC, Croxall JP, Reid K (2003a) Interannual variation in the diets of two albatross species breeding at South Georgia: implications for breeding performance. Ibis 145:593–610. doi:10.1046/j.1474-919X.2003.00196.x

    Article  Google Scholar 

  • Xavier JC, Croxall JP, Trathan PN, Rodhouse PG (2003b) Interannual variation in the cephalopod component of the diet of the wandering albatross, Diomedea exulans breeding at Bird Island, South Georgia. Mar Biol 142:611–622. doi:10.1007/s00227-002-0962-y

    Google Scholar 

  • Xavier JC, Croxall JP, Trathan PN, Wood AG (2003c) Feeding strategies and diets of breeding grey-headed and wandering albatrosses at South Georgia. Mar Biol 143:221–232. doi:10.1007/s00227-003-1049-0

    Article  Google Scholar 

  • Xavier JC, Trathan PN, Croxall JP, Wood AG, Podestá G, Rodhouse PG (2004) Foraging ecology and interactions with fisheries of wandering albatrosses (Diomedea exulans) breeding at South Georgia. Fish Oceanogr 13:324–344. doi:10.1111/j.1365-2419.2004.00298.x

    Article  Google Scholar 

  • Xavier JC, Croxall JP, Cresswell KA, Burger AE (2005) Boluses: an effective method for assessing the proportions of cephalopods in the diet of albatrosses. The Auk 122:1182–1190. doi:10.1642/0004-8038(2005)122[1182:BAEMFA]2.0.CO;2

    Article  Google Scholar 

  • Xavier JC, Tarling GA, Croxall JP (2006) Determining prey distribution patterns from stomach-contents of satellite-tracked high-predators of the Southern Ocean. Ecography 29:260–272. doi:10.1111/j.2006.0906-7590.04525.x

    Article  Google Scholar 

  • Xavier JC, Phillips RA, Cherel Y (2011) Cephalopods in marine predator diet assessments: why identifying upper and lower beaks is important. ICES J Mar Sci 68:1857–1864. doi:10.1093/icesjms/fsr103

    Article  Google Scholar 

  • Xavier JC, Louzao M, Thorpe SE, Ward P, Hill C, Roberts D, Croxall JP, Phillips RA (2013) Seasonal changes in the diet and feeding behaviour of a top predator indicate a flexible response to deteriorating oceanographic conditions. Mar Biol 160:1597–1606. doi:10.1007/s00227-013-2212-x

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Derren Fox, Stacey Adlard and Ewan Edwards at Bird Island research station for helping with sample collection in winter 2009, and Janet Silk for creating Fig. 1.This research was supported by the Ministry of Science and Higher Education, Portugal (Fundação para a Ciência e a Tecnologia), the British Antarctic Survey and the Tinker Foundation, under the research programs CEPH, SCAR AnT-ERA, PROPOLAR and ICED. This study represents a contribution to the Ecosystems component of the British Antarctic Survey Polar Science for Planet Earth Programme, funded by The Natural Environment Research Council.

Author information

Authors and Affiliations

  1. MARE-Marine and Environmental Research Centre, University of Coimbra, 3001-401, Coimbra, Portugal

    Pedro M. Alvito, Filipe Ceia, Miguel Guerreiro, José Seco, Alexandra Baeta, Rui P. Vieira & José C. Xavier

  2. Laboratório Marítimo da Guia, Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Av. Nossa Senhora do Cabo, 939, 2750-374, Cascais, Portugal

    Rui Rosa

  3. British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge, CB3 0ET, UK

    Richard A. Phillips & José C. Xavier

  4. Centre d’Etudes Biologiques de Chizé, UMR 7372 du CNRS-Université de La Rochelle, BP 14, 79360, Villiers-en-Bois, France

    Yves Cherel

Authors
  1. Pedro M. Alvito
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rui Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard A. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yves Cherel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Filipe Ceia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Miguel Guerreiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. José Seco
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alexandra Baeta
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rui P. Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. José C. Xavier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pedro M. Alvito.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alvito, P.M., Rosa, R., Phillips, R.A. et al. Cephalopods in the diet of nonbreeding black-browed and grey-headed albatrosses from South Georgia. Polar Biol 38, 631–641 (2015). https://doi.org/10.1007/s00300-014-1626-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-014-1626-3

Keywords

Search

Navigation